Active suppression of leaflet emergence as a mechanism of simple leaf development

Abstract

Angiosperm leaves show extensive shape diversity and are broadly divided into two forms; simple leaves with intact lamina and compound leaves with lamina dissected into leaflets. The mechanistic basis of margin dissection and leaflet initiation has been inferred primarily by analysing compound-leaf architecture, and thus whether the intact lamina of simple leaves has the potential to initiate leaflets upon endogenous gene inactivation remains unclear. Here, we show that the CINCINNATA-like TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTORS (CIN-TCP) transcription factors activate the class II KNOTTED1-LIKE (KNOX-II) genes and the CIN-TCP and KNOX-II proteins together redundantly suppress leaflet initiation in simple leaves. Simultaneous downregulation of CIN-TCP and KNOX-II in Arabidopsis leads to the reactivation of the stemness genes KNOX-I and CUPSHAPED COTYLEDON (CUC) and triggers ectopic organogenesis, eventually converting the simple lamina to a super-compound form that appears to initiate leaflets indefinitely. Thus, a conserved developmental mechanism promotes simple leaf architecture in which CIN-TCP-KNOX-II forms a strong differentiation module that suppresses the KNOX-I-CUC network and leaflet initiation.